Role of PARP-1 as a novel transcriptional regulator of MMP-9 in diabetic retinopathy

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1863, Issue 7, 2017, Pages 1761-1769

  Mishra, Manish ^a   Kowluru, Renu A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Acetylation; Diabetic retinopathy; MMP 9; PARP 1; Transcriptional regulation

Indexed keywords

GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SIRTUIN 1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR AP 1; MMP9 PROTEIN, HUMAN; MMP9 PROTEIN, MOUSE; N-(OXO-5,6-DIHYDROPHENANTHRIDIN-2-YL)-N,N-DIMETHYLACETAMIDE HYDROCHLORIDE; PARP1 PROTEIN, HUMAN; PARP1 PROTEIN, MOUSE; PHENANTHRENE DERIVATIVE; SIRT1 PROTEIN, HUMAN; SIRT1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENDOTHELIUM CELL; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ACETYLATION; PROTEIN BINDING; PROTEIN EXPRESSION; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ACETYLATION; ANIMAL; BIOSYNTHESIS; CELL LINE; DRUG EFFECT; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PATHOLOGY; PROTEIN PROCESSING;

ACETYLATION; ANIMALS; CELL LINE; DIABETIC RETINOPATHY; HUMANS; MATRIX METALLOPROTEINASE 9; MICE; NF-KAPPA B; PHENANTHRENES; POLY (ADP-RIBOSE) POLYMERASE-1; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIRTUIN 1; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC;

EID: 85019872482     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2017.04.024     Document Type: Article

References (49)

1. Brownlee, M., The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54 (2005), 1615–1625.
2. Kowluru, R.A., Chan, P.S., Oxidative stress and diabetic retinopathy. Exp. Diabetes Res., 2007, 2007, 43603.
3. Kowluru, R.A., Role of matrix metalloproteinase-9 in the development of diabetic retinopathy and its regulation by H-Ras. Invest. Ophthalmol. Vis. Sci. 51 (2010), 4320–4326.
4. Kowluru, R.A., Mohammad, G., dos Santos, J.M., Zhong, Q., Abrogation of MMP-9 gene protects against the development of retinopathy in diabetic mice by preventing mitochondrial damage. Diabetes 60 (2011), 3023–3033.
5. Kowluru, R.A., Santos, J.M., Zhong, Q., Sirt1, a negative regulator of matrix metalloproteinase-9 in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 55 (2014), 5653–5660.
6. Santos, J.M., Tewari, S., Lin, J.Y., Kowluru, R.A., Interrelationship between activation of matrix metalloproteinases and mitochondrial dysfunction in the development of diabetic retinopathy. Biochem. Biophys. Res. Commun. 438 (2013), 760–764.
7. Robert, I., Aussems, M., Keutgens, A., Zhang, X., Hennuy, B., Viatour, P., Vanstraelen, G., Merville, M.P., Chapelle, J.P., de Leval, L., Lambert, F., Dejardin, E., Gothot, A., Chariot, A., Metalloproteinase-9 gene induction by a truncated oncogenic NF-kappaB2 protein involves the recruitment of MLL1 and MLL2 H3K4 histone methyltransferase complexes. Oncogene 28 (2009), 1626–1628.
8. Chakraborti, S., Mandal, M., Das, S., Mandal, A., Chakraborti, T., Regulation of matrix metalloproteinases: an overview. Mol. Cell. Biochem. 253 (2003), 285–303.
9. Farina, A.R., Mackay, A.R., Gelatinase B/MMP-9 in tumour pathogenesis and progression. Cancers (Basel) 6 (2014), 240–296.
10. Mishra, M., Flaga, J., Kowluru, R.A., Molecular mechanism of transcriptional regulation of matrix metalloproteinase-9 in diabetic retinopathy. J. Cell. Physiol. 231 (2016), 1709–1718.
11. Zhong, Q., Kowluru, R.A., Regulation of matrix metalloproteinase-9 by epigenetic modifications and the development of diabetic retinopathy. Diabetes 62 (2013), 2559–2568.
12. Abate, C., Patel, L., Rauscher, F.J. 3rd, Curran, T., Redox regulation of fos and jun DNA-binding activity in vitro. Science 249 (1990), 1157–1161.
13. Karin, M., Takahashi, T., Kapahi, P., Delhase, M., Chen, Y., Makris, C., Rothwarf, D., Baud, V., Natoli, G., Guido, F., Li, N., Oxidative stress and gene expression: the AP-1 and NF-kappaB connections. Biofactors 15 (2001), 87–89.
14. von Knethen, A., Callsen, D., Brune, B., NF-kappaB and AP-1 activation by nitric oxide attenuated apoptotic cell death in RAW 264.7 macrophages. Mol. Biol. Cell 10 (1999), 361–372.
15. Aguilar-Quesada, R., Munoz-Gamez, J.A., Martin-Oliva, D., Peralta-Leal, A., Quiles-Perez, R., Rodriguez-Vargas, J.M., Ruiz de Almodovar, M., Conde, C., Ruiz-Extremera, A., Oliver, F.J., Modulation of transcription by PARP-1: consequences in carcinogenesis and inflammation. Curr. Med. Chem. 14 (2007), 1179–1187.
16. Andreone, T.L., O'Connor, M., Denenberg, A., Hake, P.W., Zingarelli, B., Poly(ADP-ribose) polymerase-1 regulates activation of activator protein-1 in murine fibroblasts. J. Immunol. 170 (2003), 2113–2120.
17. Hassa, P.O., Haenni, S.S., Buerki, C., Meier, N.I., Lane, W.S., Owen, H., Gersbach, M., Imhof, R., Hottiger, M.O., Acetylation of poly(ADP-ribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NF-kappaB-dependent transcription. J. Biol. Chem. 280 (2005), 40450–40464.
18. Zerfaoui, M., Errami, Y., Naura, A.S., Suzuki, Y., Kim, H., Ju, J., Liu, T., Hans, C.P., Kim, J.G., Abd Elmageed, Z.Y., Koochekpour, S., Catling, A., Boulares, A.H., Poly(ADP-ribose) polymerase-1 is a determining factor in Crm1-mediated nuclear export and retention of p65 NF-kappa B upon TLR4 stimulation. J. Immunol. 185 (2010), 1894–1902.
19. Kanwar, M., Kowluru, R., Role of glyceraldehyde 3-phosphate dehydrogenase in the development and progression of diabetic retinopathy. Diabetes 58 (2009), 227–234.
20. Zheng, L., Szabo, C., Kern, T.S., Poly(ADP-ribose) polymerase is involved in the development of diabetic retinopathy via regulation of nuclear factor-kappaB. Diabetes 53 (2004), 2960–2967.
21. Chen, L.F., Williams, S.A., Mu, Y., Nakano, H., Duerr, J.M., Buckbinder, L., Greene, W.C., NF-kappaB RelA phosphorylation regulates RelA acetylation. Mol. Cell. Biol. 25 (2005), 7966–7975.
22. Rajamohan, S.B., Pillai, V.B., Gupta, M., Sundaresan, N.R., Birukov, K.G., Samant, S., Hottiger, M.O., Gupta, M.P., SIRT1 promotes cell survival under stress by deacetylation-dependent deactivation of poly(ADP-ribose) polymerase 1. Mol. Cell. Biol. 29 (2009), 4116–4129.
23. Chen, W., Jump, D.B., Grant, M.B., Esselman, W.J., Busik, J.V., Dyslipidemia, but not hyperglycemia, induces inflammatory adhesion molecules in human retinal vascular endothelial cells. Invest. Ophthalmol. Vis. Sci. 44 (2003), 5016–5022.
24. Mishra, M., Kowluru, R.A., Retinal mitochondrial DNA mismatch repair in the development of diabetic retinopathy, and its continued progression after termination of hyperglycemia. Invest. Ophthalmol. Vis. Sci. 55 (2014), 6960–6967.
25. Mohammad, G., Kowluru, R.A., Matrix metalloproteinase-2 in the development of diabetic retinopathy and mitochondrial dysfunction. Lab. Investig. 90 (2010), 1365–1372.
26. Tewari, S., Santos, J.M., Kowluru, R.A., Damaged mitochondrial DNA replication system and the development of diabetic retinopathy. Antioxid. Redox Signal. 17 (2012), 492–504.
27. Kowluru, R.A., Shan, Y., Mishra, M., Dynamic DNA methylation of matrix metalloproteinase-9 in the development of diabetic retinopathy. Lab. Investig. 96 (2016), 1040–1049.
28. Rodriguez, M.I., Peralta-Leal, A., O'Valle, F., Rodriguez-Vargas, J.M., Gonzalez-Flores, A., Majuelos-Melguizo, J., Lopez, L., Serrano, S., de Herreros, A.G., Rodriguez-Manzaneque, J.C., Fernandez, R., Del Moral, R.G., de Almodovar, J.M., Oliver, F.J., PARP-1 regulates metastatic melanoma through modulation of vimentin-induced malignant transformation. PLoS Genet., 9, 2013, e1003531.
29. Kanwar, M., Kowluru, R.A., Diabetes regulates small molecular weight G-protein, H-Ras, in the microvasculature of the retina: implication in the development of retinopathy. Microvasc. Res. 76 (2008), 189–193.
30. Mishra, M., Kowluru, R.A., Epigenetic modification of mitochondrial DNA in the development of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 56 (2015), 5133–5142.
31. Zhong, Q., Mishra, M., Kowluru, R.A., Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 54 (2013), 3941–3948.
32. Santos, J.M., Mishra, M., Kowluru, R.A., Posttranslational modification of mitochondrial transcription factor A in impaired mitochondria biogenesis: implications in diabetic retinopathy and metabolic memory phenomenon. Exp. Eye Res. 121 (2014), 168–177.
33. Hassa, P.O., Hottiger, M.O., The functional role of poly(ADP-ribose)polymerase 1 as novel coactivator of NF-kappaB in inflammatory disorders. Cell. Mol. Life Sci. 59 (2002), 1534–1553.
34. Hassa, P.O., Buerki, C., Lombardi, C., Imhof, R., Hottiger, M.O., Transcriptional coactivation of nuclear factor-kappaB-dependent gene expression by p300 is regulated by poly(ADP)-ribose polymerase-1. J. Biol. Chem. 278 (2003), 45145–45153.
35. Kraus, W.L., Lis, J.T., PARP goes transcription. Cell 113 (2003), 677–683.
36. Kern, T.S., Tang, J., Mizutani, M., Kowluru, R., Nagraj, R., Lorenzi, M., Response of capillary cell death to aminoguanidine predicts the development of retinopathy: comparison of diabetes and galactosemia. Invest. Ophthalmol. Vis. Sci. 41 (2000), 3972–3978.
37. Kowluru, R.A., Abbas, S.N., Diabetes-induced mitochondrial dysfunction in the retina. Invest. Ophthalmol. Vis. Sci. 44 (2003), 5327–5334.
38. Kowluru, R.A., Kanwar, M., Oxidative stress and the development of diabetic retinopathy: contributory role of matrix metalloproteinase-2. Free Radic. Biol. Med. 46 (2009), 1677–1685.
39. Mizutani, M., Kern, T.S., Lorenzi, M., Accelerated death of retinal microvascular cells in human and experimental diabetic retinopathy. J. Clin. Invest. 97 (1996), 2883–2890.
40. Valenzuela, M.T., Guerrero, R., Nunez, M.I., Ruiz De Almodovar, J.M., Sarker, M., de Murcia, G., Oliver, F.J., PARP-1 modifies the effectiveness of p53-mediated DNA damage response. Oncogene 21 (2002), 1108–1116.
41. Fossati, S., Formentini, L., Wang, Z.Q., Moroni, F., Chiarugi, A., Poly(ADP-ribosyl)ation regulates heat shock factor-1 activity and the heat shock response in murine fibroblasts. Biochem. Cell Biol. 84 (2006), 703–712.
42. Krishnakumar, R., Kraus, W.L., PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol. Cell 39 (2010), 736–749.
43. Kassan, M., Choi, S.K., Galan, M., Bishop, A., Umezawa, K., Trebak, M., Belmadani, S., Matrougui, K., Enhanced NF-kappaB activity impairs vascular function through PARP-1-, SP-1-, and COX-2-dependent mechanisms in type 2 diabetes. Diabetes 62 (2013), 2078–2087.
44. Obrosova, I.G., Li, F., Abatan, O.I., Forsell, M.A., Komjati, K., Pacher, P., Szabo, C., Stevens, M.J., Role of poly(ADP-ribose) polymerase activation in diabetic neuropathy. Diabetes 53 (2004), 711–720.
45. Szabo, C., Biser, A., Benko, R., Bottinger, E., Susztak, K., Poly(ADP-ribose) polymerase inhibitors ameliorate nephropathy of type 2 diabetic Leprdb/db mice. Diabetes 55 (2006), 3004–3012.
46. Abu El-Asrar, A.M., Mohammad, G., Nawaz, M.I., Siddiquei, M.M., Van den Eynde, K., Mousa, A., De Hertogh, G., Opdenakker, G., Relationship between vitreous levels of matrix metalloproteinases and vascular endothelial growth factor in proliferative diabetic retinopathy. PLoS One, 8, 2013, e85857.
47. Martin-Oliva, D., Aguilar-Quesada, R., O'Valle, F., Munoz-Gamez, J.A., Martinez-Romero, R., Garcia Del Moral, R., Ruiz de Almodovar, J.M., Villuendas, R., Piris, M.A., Oliver, F.J., Inhibition of poly(ADP-ribose) polymerase modulates tumor-related gene expression, including hypoxia-inducible factor-1 activation, during skin carcinogenesis. Cancer Res. 66 (2006), 5744–5756.
48. Hassa, P.O., Covic, M., Hasan, S., Imhof, R., Hottiger, M.O., The enzymatic and DNA binding activity of PARP-1 are not required for NF-kappa B coactivator function. J. Biol. Chem. 276 (2001), 45588–45597.
49. Luna, A., Aladjem, M.I., Kohn, K.W., SIRT1/PARP1 crosstalk: connecting DNA damage and metabolism. Genome Integr., 4, 2013, 6.